Structural basis of substrate binding specificity revealed by the crystal structures of polyamine receptors SpuD and SpuE from pseudomonas aeruginosa

Journal of Molecular Biology

Volumn 416, Issue 5, 2012, Pages 697-712

  Wu, Donghui ^a,b   Lim, Siew Choo ^a,c   Dong, Yihu ^a   Wu, Jien ^a   Tao, Fei ^a   Zhou, Lian ^a   Zhang, Lian Hui ^a,b   Song, Haiwei ^a,b  

^a INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

ligand induced conformational change; polyamine binding; SpuD; SpuE; type III secretion system

Indexed keywords

BACTERIAL PROTEIN; BINDING PROTEIN; PHENYLALANINE; PROTEIN POTD; PROTEIN POTF; PROTEIN SPUD; PROTEIN SPUE; PUTRESCINE; RECEPTOR; SPERMIDINE; TRYPTOPHAN; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; BETA SHEET; BINDING AFFINITY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ESCHERICHIA COLI; GENE EXPRESSION; ISOTHERMAL TITRATION CALORIMETRY; LIGAND BINDING; MOLECULAR RECOGNITION; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PSEUDOMONAS AERUGINOSA; RECEPTOR BINDING; STRUCTURE ANALYSIS; TYPE III SECRETION SYSTEM;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; MAMMALIA; PSEUDOMONAS AERUGINOSA;

EID: 84862778515     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2012.01.010     Document Type: Article

References (46)

1. Tabor H. The protective effect of spermine and other polyamines against heat denaturation of deoxyribonucleic acid Biochemistry 1 1962 496 501
2. Bloomfield V.A. DNA condensation by multivalent cations Biopolymers 44 1997 269 282
3. Shah N., Thomas T., Shirahata A., Sigal L.H., and Thomas T.J. Activation of nuclear factor kappaB by polyamines in breast cancer cells Biochemistry 38 1999 14763 14774
4. Thomas T., Gallo M.A., Klinge C.M., and Thomas T.J. Polyamine-mediated conformational perturbations in DNA alter the binding of estrogen receptor to poly(dG-m5dC).poly(dG-m5dC) and a plasmid containing the estrogen response element J. Steroid. Biochem. Mol. Biol. 54 1995 89 99
5. Igarashi K., Kashiwagi K., Kishida K., Watanabe Y., Kogo A., and Hirose S. Defect in the split proteins of 30-S ribosomal subunits and under-methylation of 16-S ribosomal RNA in a polyamine-requiring mutant of Escherichia coli grown in the absence of polyamines Eur. J. Biochem. 93 1979 345 353 (Pubitemid 9230638)
6. Kakegawa T., Hirose S., Kashiwagi K., and Igarashi K. Effect of polyamines on in vitro reconstitution of ribosomal subunits Eur. J. Biochem. 158 1986 265 269
7. Kusama-Eguchi K., Watanabe S., Irisawa M., Watanabe K., and Igarashi K. Correlation between spermine stimulation of rat liver Ile-tRNA formation and structural change of the acceptor stem by spermine Biochem. Biophys. Res. Commun. 177 1991 745 750
8. Peng Z., Kusama-Eguchi K., Watanabe S., Ito K., Watanabe K., Nomoto Y., and Igarashi K. Responsibility of tRNA(Ile) for spermine stimulation of rat liver Ile-tRNA formation Arch. Biochem. Biophys. 279 1990 138 145 (Pubitemid 20149784)
9. Wang J.Y. Polyamines and mRNA stability in regulation of intestinal mucosal growth Amino Acids 33 2007 241 252
10. Cochet C., and Chambaz E.M. Polyamine-mediated protein phosphorylations: a possible target for intracellular polyamine action Mol. Cell. Endocrinol. 30 1983 247 266 (Pubitemid 13103528)
11. Tome M.E., Fiser S.M., Payne C.M., and Gerner E.W. Excess putrescine accumulation inhibits the formation of modified eukaryotic initiation factor 5A (eIF-5A) and induces apoptosis Biochem. J. 328 1997 847 854 (Pubitemid 28005785)
12. Heby O. Role of polyamines in the control of cell proliferation and differentiation Differentiation 19 1981 1 20 (Pubitemid 11091193)
13. Packham G., and Cleveland J.L. Ornithine decarboxylase is a mediator of c-Myc-induced apoptosis Mol. Cell. Biol. 14 1994 5741 5747 (Pubitemid 24264402)
14. Thomas T., Gunnia U.B., Yurkow E.J., Seibold J.R., and Thomas T.J. Inhibition of calcium signalling in murine splenocytes by polyamines: differential effects on CD4 and CD8 T-cells Biochem. J. 291 1993 375 381 (Pubitemid 23127016)
15. Heby O. DNA methylation and polyamines in embryonic development and cancer Int. J. Dev. Biol. 39 1995 737 757 (Pubitemid 26056345)
16. Bachrach U. Polyamines and cancer: minireview article Amino Acids 26 2004 307 309 (Pubitemid 39093131)
17. Gilmour S.K. Polyamines and nonmelanoma skin cancer Toxicol. Appl. Pharmacol. 224 2007 249 256 (Pubitemid 47575671)
18. Palavan-Unsal N., Aloglu-Senturk S.M., and Arsan D. The function of poliamine metabolism in prostate cancer Exp. Oncol. 28 2006 178 186 (Pubitemid 44735906)
19. Tyms A.S., Williamson J.D., and Bacchi C.J. Polyamine inhibitors in antimicrobial chemotherapy J. Antimicrob. Chemother. 22 1988 403 427 (Pubitemid 18264809)
20. Tam R., and Saier M.H. Jr Structural, functional, and evolutionary relationships among extracellular solute-binding receptors of bacteria Microbiol. Rev. 57 1993 320 346 (Pubitemid 23170095)
21. Furuchi T., Kashiwagi K., Kobayashi H., and Igarashi K. Characteristics of the gene for a spermidine and putrescine transport system that maps at 15 min on the Escherichia coli chromosome J. Biol. Chem. 266 1991 20928 20933 (Pubitemid 21908553)
22. Kashiwagi K., Hosokawa N., Furuchi T., Kobayashi H., Sasakawa C., Yoshikawa M., and Igarashi K. Isolation of polyamine transport-deficient mutants of Escherichia coli and cloning of the genes for polyamine transport proteins J. Biol. Chem. 265 1990 20893 20897 (Pubitemid 120014094)
23. Higgins C.F. ABC transporters: from microorganisms to man Annu. Rev. Cell. Biol. 8 1992 67 113 (Pubitemid 23000992)
24. Talbot G.H., Bradley J., Edwards J.E. Jr, Gilbert D., Scheld M., Bartlett J.G. Antimicrobial Availability Task Force of the Infectious Diseases Society of America Bad bugs need drugs: an update on the development pipeline from the Antimicrobial Availability Task Force of the Infectious Diseases Society of America Clin. Infect. Dis. 42 2006 657 668 (Pubitemid 43271379)
25. Lu C.D., Itoh Y., Nakada Y., and Jiang Y. Functional analysis and regulation of the divergent spuABCDEFGH-spuI operons for polyamine uptake and utilization in Pseudomonas aeruginosa PAO1 J. Bacteriol. 184 2002 3765 3773 (Pubitemid 34705431)
26. Kwon D.H., and Lu C.D. Polyamines induce resistance to cationic peptide, aminoglycoside, and quinolone antibiotics in Pseudomonas aeruginosa PAO1 Antimicrob. Agents. Chemother. 50 2006 1615 1622
27. Zhou L., Wang J., and Zhang L.H. Modulation of bacterial type III secretion system by a spermidine transporter dependent signaling pathway PLoS One 2 2007 e1291
28. Sugiyama S., Matsuo Y., Maenaka K., Vassylyev D.G., Matsushima M., and Kashiwagi K. The 1.8-Å X-ray structure of the Escherichia coli PotD protein complexed with spermidine and the mechanism of polyamine binding Protein Sci. 5 1996 1984 1990
29. Sugiyama S., Vassylyev D.G., Matsushima M., Kashiwagi K., Igarashi K., and Morikawa K. Crystal structure of PotD, the primary receptor of the polyamine transport system in Escherichia coli J. Biol. Chem. 271 1996 9519 9525 (Pubitemid 26139929)
30. Vassylyev D.G., Tomitori H., Kashiwagi K., Morikawa K., and Igarashi K. Crystal structure and mutational analysis of the Escherichia coli putrescine receptor. Structural basis for substrate specificity J. Biol. Chem. 273 1998 17604 17609 (Pubitemid 28355097)
31. Machius M., Brautigam C.A., Tomchick D.R., Ward P., Otwinowski Z., and Blevins J.S. Structural and biochemical basis for polyamine binding to the Tp0655 lipoprotein of Treponema pallidum: putative role for Tp0655 (TpPotD) as a polyamine receptor J. Mol. Biol. 373 2007 681 694 (Pubitemid 47489786)
32. Sharff A.J., Rodseth L.E., Spurlino J.C., and Quiocho F.A. Crystallographic evidence of a large ligand-induced hinge-twist motion between the two domains of the maltodextrin binding protein involved in active transport and chemotaxis Biochemistry 31 1992 10657 10663
33. Spurlino J.C., Lu G.Y., and Quiocho F.A. The 2.3-Å resolution structure of the maltose- or maltodextrin-binding protein, a primary receptor of bacterial active transport and chemotaxis J. Biol. Chem. 266 1991 5202 5219 (Pubitemid 21909478)
34. Matthews H.R. Polyamines, chromatin structure and transcription BioEssays 15 1993 561 566
35. Oldham M.L., Khare D., Quiocho F.A., Davidson A.L., and Chen J. Crystal structure of a catalytic intermediate of the maltose transporter Nature 450 2007 515 521 (Pubitemid 350190241)
36. Khare D., Oldham M.L., Orelle C., Davidson A.L., and Chen J. Alternating access in maltose transporter mediated by rigid-body rotations Mol. Cell 33 2009 528 536
37. Oldham M.L., and Chen J. Crystal structure of the maltose transporter in a pretranslocation intermediate state Science 332 2011 1202 1205
38. Sambrook J., Fritsch E.F., and Maniatis T. Molecular Cloning: A Laboratory Manual 1987 Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY
39. CCP4 The CCP4 suite: programs for protein crystallography Acta Crystallogr., Sect. D: Biol. Crystallogr. 50 1994 760 763
40. Kabsch W. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants J. Appl. Crystallogr. 26 1993 795 800
41. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics Acta Crystallogr., Sect. D: Biol. Crystallogr. 60 2004 2126 2132 (Pubitemid 41742764)
42. Murshudov G.N., Vagin A.A., and Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr., Sect. D: Biol. Crystallogr. 53 1997 240 255 (Pubitemid 27235885)
43. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., and Grosse-Kunstleve R.W. Crystallography & NMR system: a new software suite for macromolecular structure determination Acta Crystallogr., Sect. D: Biol. Crystallogr. 54 1998 905 921
44. Schneider T.R., and Sheldrick G.M. Substructure solution with SHELXD Acta Crystallogr., Sect. D: Biol. Crystallogr. 58 2002 1772 1779 (Pubitemid 35169744)
45. Perrakis A., Morris R., and Lamzin V.S. Automated protein model building combined with iterative structure refinement Nat. Struct. Biol. 6 1999 458 463 (Pubitemid 29218016)
46. Laskowski R.A., MacArthur M.W., Moss D.S., and Thornton J.M. PROCHECK: a program to check the stereochemical quality of protein structures J. Appl. Crystallogr. 26 1993 283 291